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Biodiversity of the Natural Enemies of Aphids (Hemiptera: Aphididae) in Northwest Turkey

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Biodiversity of the Natural Enemies of Aphids (Hemiptera: Aphididae) in Northwest Turkey Phytoparasitica https://doi.org/10.1007/s12600-019-00781-8 Biodiversity of the natural enemies of aphids (Hemiptera: Aphididae) in Northwest Turkey Şahin Kök & Željko Tomanović & Zorica Nedeljković & Derya Şenal & İsmail Kasap Received: 25 April 2019 /Accepted: 19 December 2019 # Springer Nature B.V. 2020 Abstract In the present study, the natural enemies of (Hymenoptera), as well as eight other generalist natural aphids (Hemiptera: Aphididae) and their host plants in- enemies. In these interactions, a total of 37 aphid-natural cluding herbaceous plants, shrubs and trees were enemy associations–including 19 associations of analysed to reveal their biodiversity and disclose Acyrthosiphon pisum (Harris) with natural enemies, 16 tritrophic associations in different habitats of the South associations of Therioaphis trifolii (Monell) with natural Marmara region of northwest Turkey. As a result of field enemies and two associations of Aphis craccivora Koch surveys, 58 natural enemy species associated with 43 with natural enemies–were detected on Medicago sativa aphids on 58 different host plants were identified in the L. during the sampling period. Similarly, 12 associations region between March of 2017 and November of 2018. of Myzus cerasi (Fabricius) with natural enemies were In 173 tritrophic natural enemy-aphid-host plant interac- revealed on Prunus avium (L.), along with five associa- tions including association records new for Europe and tions of Brevicoryne brassicae (Linnaeus) with natural Turkey, there were 21 representatives of the family enemies (including mostly parasitoid individuals) on Coccinellidae (Coleoptera), 14 of the family Syrphidae Brassica oleracea L. Also in the study, reduviids of the (Diptera) and 15 of the subfamily Aphidiinae species Zelus renardii (Kolenati) are reported for the first time as new potential aphid biocontrol agents in Turkey. The results of field surveys show that the natural enemies Ş. Kök (*) : İ.Kasap of aphids have high biodiversity, which should be con- Department of Plant Protection, Faculty of Agriculture, Çanakkale sidered in the management of biological pest control. Onsekiz Mart University, TR-17020 Çanakkale, Turkey e-mail: [email protected] Keywords Biological control . Aphididae . e-mail: [email protected] Coccinellidae . Syrphinae . Aphidiinae . South Marmara Ž. Tomanović Faculty of Biology, Institute of Zoology, University of Belgrade, Studenstki trg 16, Belgrade 11000, Serbia Introduction Z. Nedeljković BioSense Institute-Research Institute for Information Technologies in Biosystems, Dr Zorana Đinđića1,Novi As one of the most important of agricultural pests, Sad 21000, Serbia aphids (Hemiptera, Aphididae) cause severe significant economic losses and are distributed in most terrestrial D. Şenal Department of Plant Protection, Faculty of Agriculture and Natural ecosystems throughout the world. They damage agri- Sciences, Bilecik Şeyh Edebali University, cultural crops, forest plants and shade trees, especially in TR-11230 Bilecik, Turkey temperate regions, as a result of sap-sucking, honeydew Phytoparasitica secretion and transmission of phytopathogenic viruses habitats of the South Marmara region of northwest (Alford 2011; Diehl et al. 2013). Turkey, which is an important crossroad between Eu- Natural enemies, including specialist and generalist rope and Asia and has a rich and diverse flora and fauna. species, play a very important role in suppressing pop- ulations of aphids and other arthropod herbivores (Symondson et al. 2002;Luetal.2012), Such natural Material and methods enemies affect at least 50% of all aphid species on the surface of the earth (Waage 1991). Up to now, about Sampling area 2000 arthropods, generally consisting of parasitoid spe- cies, have been determined as biological control agents Our sampling area, the South Marmara region in north- worldwide (van Lenteren et al. 2006). Aphids are usu- west Turkey, consists of the Çanakkale and Balıkesir ally attacked by natural enemies such as parasitoids, Provinces, which constitute an important link between predators and some pathogens. Of these, both the larvae Europe and Asia. This area includes 3% of Turkey’s and the adult stages of coccinellid species are preda- land, with a surface area of 783.562 km2, and it is an ceous on aphids, while only the larval stages of syrphids outstanding region in terms of agricultural production. and chrysopids are predaceous on them. Also among The region has a continental climate in the southeastern parasitoids, species belonging to the family Braconidae parts, milder climate in parts close to the coastal area and (especially members of the subfamily Aphidiinae) de- Mediterranean climate in regions of the gulf and islands. velop as solitary endoparasitoids on aphid populations The sampling area also includes wilderness areas such (Völkl et al. 2007). as the Edremit Gulf, Biga Peninsula, Gallipoli Peninsula Surveying the biodiversity of natural enemies of and Kaz Dağları (Ida Mountains), which are known to herbivore pests in both agricultural and natural habitats have a high degree of endemic floristic and faunistic is quite important from the standpoint of planning bio- diversity (Özhatay and Özhatay 2005). logical control strategies. A richness of natural enemies makes possible stronger biological control in all habitats Collection and identification of aphids and their natural (Letourneau et al. 2009; Griffin et al. 2013; Katano et al. enemies 2015). When the taxonomic distance between natural enemies on herbivore pests was high, the effect of this Specimens of aphids and their natural enemies were phenomenon was likewise positive (Griffin et al. 2013). collected from their host plants, including herbaceous However, greater diversity of natural enemies can lead plants, shrubs and trees in different habitats such as to more ineffective pest control in agricultural habitats cultivated (simple landscapes-1), uncultivated (Snyder and Wise 2001; Montoya et al. 2003). (complex landscapes-2) and urban areas (3) in the In addition, the nature of associations of aphid and Çanakkale and Balıkesir Provinces in northwest Turkey their host plants in different habitats can regulate the between March of 2017 and November of 2018. Ac- efficacy of influence exerted by specialist and generalist cordingly, all samples were marked in the catalogue of natural enemies on aphid populations. According to the associations. Sufficient numbers of apterous and alate hypothesis of host physiological phenotype, host plants specimens of aphids were transferred with a soft brush that are nutrient-rich and short-lived tend to increase the to Eppendorf tubes containing 70% ethyl alcohol for density of aphids (Cronin et al. 2010), as in the case of identification. The aphid specimens were identified by populations of other nitrogen-limited herbivores the first author using a LEICA DM 2500 microscope (Mattson 1980), because host plants with a great amount with a mounted HD camera and LAS software (version of nitrogen have a positive effect on the development of 4.1) according to Blackman and Eastop (2006, 2018) aphid populations (Schütz et al. 2008). In view of the and Kök et al. (2016); Kök and Kasap (2019). Adults of aforementioned considerations, the biodiversity of nat- natural enemies, especially ladybirds, hoverflies and ural enemies and their interactions with both pests and generalist predators such as representatives of host plants were here investigated in detail so as to better Hemiptera, Dermaptera and Neuroptera, were collected understand enemy-herbivore-host plant associations. from host plants infested with aphids by visual and hand The aim of the present study was to reveal biodiver- searching using sweep nets and suction tubes, after sity of the natural enemies of pest aphids in different which they were brought to the laboratory in plastic Phytoparasitica boxes and glass jars for preparation and identification. hoverflies, are one of the most common known natural For sampling of predator larvae and parasitoids, differ- enemies of aphid populations (Chambers 1988) and are ent parts of aphid-infested plants including predator important agents for the biological control of many pests larvae and mummified aphids were brought in the same under both agricultural and greenhouse conditions boxes to the laboratory for emergence of adult speci- (Pineda and García 2008; Leroy et al. 2010; Amorós- mens. The larvae of predators were kept until they were Jiménez et al. 2012). The most effective of them, larvae adults in the aphid-containing plastic boxes, the upper of the species Episyrphus balteatus de Geer, feed on part of which was covered with a net. For parasitoid about 100 aphid species throughout the world (Sadeghi emergence, mummified individuals in aphid colonies on and Gilbert 2000). In the same vein, Bayrak and Hayat the host plants were put in plastic bottles and kept in (2008)statedthatE. balteatus preys on 33 aphid species laboratory conditions (22.5 °C, 65% humidity, 16:8 L:D and is common in many regions of Turkey. Similarly, photoperiod). After the emergence of adult predators we found that the larvae of this hoverfly species feed on and parasitoids, the specimens of natural enemies of 10 aphid species harmful to many cultivated plants and aphids were sent to competent experts for identification. are commonly encountered in our study area. Specimens belonging to the subfamily Aphidiinae Among the most notable details in the catalogue of (Braconidae) and families Syrphidae and
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